Studies on the molecular regulation of nutrient supplementation in carnivorous Nepenthes
All organisms on earth are forced by environmental challenges for millions of years to either adapt, or escape from inhospitable habitats. Being sessile organisms, adaptation is the only alternative for plants. High plasticity in plant metabolism, biochemical and signaling pathways, and morphological variations promote the performance of plants under stressful environmental conditions. Plants also successfully co-exist with other organisms such as microbes or insects. As an adaptation mechanism for nutrient limited habitats and soil, carnivory has developed from plant-insect interactions. Most terrestrial carnivorous plants such as Nepenthes, Dionaea and Drosera use diverse trapping organs; however they all specialize in insect prey digestion to have access to prey-derived nutrients. Carnivorous plant of the genus Nepenthes with over 120 species uses so-called pitchers, which are metamorphosed leaf organs with digestive fluid inside. Identified protein compositions of the digestive fluid are categorized in the families of pathogenesis related (PR) proteins. Only few species of Nepenthes developed mutualistic relationships with mammals for nitrogen supplementation allowing further coprophagous specialization. Here, we show the following results: Insect prey as well as chitin is able to first induce jasmonate phytohormones, which in turn can induce genes of digestive enzymes such as a chitinase and a protease, nepenthesin. For the latter, prey- and chitin-induced activity was also detected in the pitcher fluid. Moreover, external jasmonic acid application was sufficient to induce proteolytic activity of the fluid, indicating the important role of jasmonate signaling in prey-digestion related gene expression. Putative cis-acting regulatory elements are observed on the promoter regions of selected PR genes of the digestive fluid proteins. Some of those potential promoter elements are known to be involved in plant defense regulations. Apart from prey-derived nutrient acquisition, Nepenthes was also capable to metabolize 15N-enriched urea and following which the nitrogen is distributed within the plant. Exactly this ability of the plant, which is facilitated by the enzyme urease, allowed further specialization, namely coprophagy. In such case, the plants benefit from animal defecation. Urease genes from coprophagous and carnivorous Nepenthes species were cloned and functionally expressed. A comprehensive phylogenetic analysis for eukaryotic ureases, including Nepenthes and five other carnivorous plants taxa, identified them as canonical ureases and reflects the plant phylogeny. Overall, the results of my thesis demonstrate the ability of Nepenthes plants to shape existing pathways in favor of carnivory or even coprophagy. It, furthermore, confirms the hypothesis that carnivory has evolved from plant defense strategies and that this lifestyle seems to have evolved convergently in the different taxa of carnivorous plants.
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